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Assessment of Hydrocarbon Degradation Potential in Microbial Communities in Arctic Sea Ice - PubMed

  • ️Sat Jan 01 2022

Assessment of Hydrocarbon Degradation Potential in Microbial Communities in Arctic Sea Ice

Angela Peeb et al. Microorganisms. 2022.

Abstract

The anthropogenic release of oil hydrocarbons into the cold marine environment is an increasing concern due to the elevated usage of sea routes and the exploration of new oil drilling sites in Arctic areas. The aim of this study was to evaluate prokaryotic community structures and the genetic potential of hydrocarbon degradation in the metagenomes of seawater, sea ice, and crude oil encapsulating the sea ice of the Norwegian fjord, Ofotfjorden. Although the results indicated substantial differences between the structure of prokaryotic communities in seawater and sea ice, the crude oil encapsulating sea ice (SIO) showed increased abundances of many genera-containing hydrocarbon-degrading organisms, including Bermanella, Colwellia, and Glaciecola. Although the metagenome of seawater was rich in a variety of hydrocarbon degradation-related functional genes (HDGs) associated with the metabolism of n-alkanes, and mono- and polyaromatic hydrocarbons, most of the normalized gene counts were highest in the clean sea ice metagenome, whereas in SIO, these counts were the lowest. The long-chain alkane degradation gene almA was detected from all the studied metagenomes and its counts exceeded ladA and alkB counts in both sea ice metagenomes. In addition, almA was related to the most diverse group of prokaryotic genera. Almost all 18 good- and high-quality metagenome-assembled genomes (MAGs) had diverse HDGs profiles. The MAGs recovered from the SIO metagenome belonged to the abundant taxa, such as Glaciecola, Bermanella, and Rhodobacteracea, in this environment. The genera associated with HDGs were often previously known as hydrocarbon-degrading genera. However, a substantial number of new associations, either between already known hydrocarbon-degrading genera and new HDGs or between genera not known to contain hydrocarbon degraders and multiple HDGs, were found. The superimposition of the results of comparing HDG associations with taxonomy, the HDG profiles of MAGs, and the full genomes of organisms in the KEGG database suggest that the found relationships need further investigation and verification.

Keywords: Arctic seawater; crude oil; hydrocarbon degradation genes; hydrocarbon-degrading organisms; prokaryotic community; sea ice; shotgun metagenomics.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1

The microbial community structure at kingdom, phylum (>1%), and class (>1%) levels based on all sequences (A,C,E), and the genus (the 20 most abundant prokaryotic genera in each metagenome) level (B,D,F) based on sequences classified as bacterial and archaeal in the metagenomes of seawater (SW), sea ice (SI), and sea ice with encapsulated crude oil (SIO). The genera-containing oil hydrocarbon-degrading organisms are marked in bold.

Figure 2
Figure 2

A Venn diagram showing unique and similar prokaryotic genera (>0.05% of prokaryotic community) in seawater (SW), sea ice (SI), and crude oil encapsulating sea ice (SIO) metagenomes. The genera-containing oil hydrocarbon-degrading organisms are marked in bold and archaeal genera are underlined in red.

Figure 3
Figure 3

Scatterplots showing ratios of normalized hydrocarbon degradation genes and gene cluster counts between metagenomes of sea ice and seawater (SI/SW) along the x-axis, and between sea ice encapsulating crude oil and sea ice (SIO/SI) along the y-axis. The ratios are shown on separate subplots for alkane degradation genes (A), genes of monocyclic and polycyclic aromatic compounds (B and C, respectively), and for genes that encode enzymes participating in the degradation pathways of various types of hydrocarbons (D). The averages of the ratios of each group are indicated by red dashed lines and standard deviations are indicated by the blue area for the x-axis and green area for the y-axis. The position of the genes and gene clusters forming tight groups around the crossing of the group averages on the subplots B and D are shown in zoomed windows.

Figure 4
Figure 4

Prokaryotic genera associated with alkane degradation genes and gene clusters in the metagenomes of seawater (SW), sea ice (SI), and sea ice encapsulating crude oil (SIO). Genera without stars correspond to taxa previously shown to involve hydrocarbon degraders. Black stars mark genera that have not been previously shown to contain hydrocarbon degraders in the literature and that the genomes (KEGG BRITE) lack genes annotated to the hydrocarbon degradation genes (HDGs); green stars mark genera that contain organisms with genomes which (KEGG BRITE) have similar hydrocarbon degradation genes (HDGs); red stars mark genera that contain organisms possessing HDGs (KEGG BRITE) different from the current findings; and blue stars mark genera with representatives which were missing from KEGG BRITE.

Figure 5
Figure 5

Prokaryotic genera (100 of the most abundant across all metagenomes) associated with monoaromatic hydrocarbon degradation genes and gene clusters in the metagenomes of seawater (SW), sea ice (SI), and sea ice encapsulating crude oil (SIO). Genera without stars correspond to taxa previously shown to involve hydrocarbon degraders. Black stars mark genera that have not been previously shown to contain hydrocarbon degraders in the literature and that the genomes (KEGG BRITE) lack genes annotated to the hydrocarbon degradation genes (HDGs); red stars mark genera that contain organisms possessing HDGs (KEGG BRITE) different from the current findings; and blue stars mark genera with representatives which were missing from KEGG BRITE.

Figure 6
Figure 6

Prokaryotic genera (100 of the most abundant across all metagenomes) associated with polycyclic aromatic hydrocarbon degradation genes and gene clusters in metagenomes of seawater (SW), sea ice (SI), and sea ice encapsulating crude oil (SIO). Genera without stars correspond to taxa previously shown to involve hydrocarbon degraders. Black stars mark genera that have not been previously shown to contain hydrocarbon degraders in the literature and that the genomes (KEGG BRITE) lack genes annotated to the hydrocarbon degradation genes (HDGs); green stars mark genera that contain organisms with genomes which (KEGG BRITE) have similar hydrocarbon degradation genes (HDGs); red stars mark genera that contain organisms possessing HDGs (KEGG BRITE) different from the current findings; and blue stars mark genera with representatives which were missing from KEGG BRITE.

Figure 7
Figure 7

Prokaryotic genera (100 of the most abundant across all metagenomes) associated with the degradation genes of various types of hydrocarbons and gene clusters in the metagenomes of seawater (SW), sea ice (SI), and sea ice encapsulating crude oil (SIO). Genera without stars correspond to taxa previously shown to involve hydrocarbon degraders. Black stars mark genera that have not been previously shown to contain hydrocarbon degraders in the literature and that the genomes (KEGG BRITE) lack genes annotated to the hydrocarbon degradation genes (HDGs); green stars mark genera that contain organisms with genomes which (KEGG BRITE) have similar hydrocarbon degradation genes (HDGs); red stars mark genera that contain organisms possessing HDGs (KEGG BRITE) different from the current findings; and blue stars mark genera with representatives which were missing from KEGG BRITE.

Figure 8
Figure 8

The clustering (relatedness analysis) of MAG sequences (A), and the presence of gene clusters encoding enzymes that were involved in the degradation of the crude oil compounds detected in these MAGs (B). SW, SI, and SIO in the codes of MAGs refer to seawater, sea ice, and sea ice encapsulating crude oil, respectively, and a and b refer to bacterial or archaeal origin, respectively. The upright dotted line on subplot A distinguishes species-level similarity.

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